The Quaternary Structure of a Glycoside Hydrolase Dictates Specificity toward β-Glucans

J Biol Chem. 2016 Mar 25;291(13):7183-94. doi: 10.1074/jbc.M115.695999. Epub 2016 Jan 11.

Abstract

In the Carbohydrate-Active Enzyme (CAZy) database, glycoside hydrolase family 5 (GH5) is a large family with more than 6,000 sequences. Among the 51 described GH5 subfamilies, subfamily GH5_26 contains members that display either endo-β(1,4)-glucanase or β(1,3;1,4)-glucanase activities. In this study, we focused on the GH5_26 enzyme fromSaccharophagus degradans(SdGluc5_26A), a marine bacterium known for its capacity to degrade a wide diversity of complex polysaccharides.SdGluc5_26A displays lichenase activity toward β(1,3;1,4)-glucans with a side cellobiohydrolase activity toward β(1,4)-glucans. The three-dimensional structure ofSdGluc5_26A adopts a stable trimeric quaternary structure also observable in solution. The N-terminal region ofSdGluc5_26A protrudes into the active site of an adjacent monomer. To understand whether this occupation of the active site could influence its activity, we conducted a comprehensive enzymatic characterization ofSdGluc5_26A and of a mutant truncated at the N terminus. Ligand complex structures and kinetic analyses reveal that the N terminus governs the substrate specificity ofSdGluc5_26A. Its deletion opens the enzyme cleft at the -3 subsite and turns the enzyme into an endo-β(1,4)-glucanase. This study demonstrates that experimental approaches can reveal structure-function relationships out of reach of current bioinformatic predictions.

Keywords: CAZyme; Saccharophagus degradans; crystallography; endoglucanase; enzyme; glycobiology; glycoside hydrolase; lichenase; oligomerization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Aquatic Organisms
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Biocatalysis
  • Catalytic Domain
  • Cellulose 1,4-beta-Cellobiosidase / chemistry*
  • Cellulose 1,4-beta-Cellobiosidase / genetics
  • Cellulose 1,4-beta-Cellobiosidase / metabolism
  • Cloning, Molecular
  • Crystallography, X-Ray
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gammaproteobacteria / chemistry*
  • Gammaproteobacteria / enzymology
  • Gene Expression
  • Glycoside Hydrolases / chemistry*
  • Glycoside Hydrolases / genetics
  • Glycoside Hydrolases / metabolism
  • Hydrolysis
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation
  • Protein Multimerization
  • Protein Structure, Quaternary
  • Protein Structure, Secondary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Substrate Specificity
  • beta-Glucans / chemistry*
  • beta-Glucans / metabolism

Substances

  • Bacterial Proteins
  • Recombinant Proteins
  • beta-Glucans
  • Glycoside Hydrolases
  • licheninase
  • Cellulose 1,4-beta-Cellobiosidase

Associated data

  • PDB/1A3H
  • PDB/1ECE
  • PDB/1H5V
  • PDB/2CKR
  • PDB/3AZT
  • PDB/4HTY
  • PDB/4HU0
  • PDB/5A8M
  • PDB/5A8N
  • PDB/5A8O
  • PDB/5A8P
  • PDB/5A8Q
  • PDB/5A94
  • PDB/5A95